Gene cluster conservation provides insight into cercosporin biosynthesis and extends production to the genus Colletotrichum

Species in the genus Cercospora cause economically
devastating diseases in sugar beet, maize, rice, soy bean and other major food
crops. Here we sequenced the
genome of the sugar beet pathogen C.
beticola and
found it encodes 63 putative secondary metabolite gene clusters,
including the cercosporin toxin biosynthesis (CTB) cluster. We show that the CTB gene cluster has experienced multiple duplications and
horizontal transfers across a spectrum of plant pathogenic fungi, including the
wide-host range Colletotrichum genus
as well as the rice pathogen Magnaporthe
oryzae. Although cercosporin biosynthesis has been thought to-date to rely
on an eight gene CTB cluster, our phylogenomic
analysis revealed gene collinearity adjacent to the established cluster in all CTB cluster-harboring species. We demonstrate
that the CTB cluster is larger than
previously recognized and includes cercosporin
facilitator protein (CFP),
previously shown to be involved with cercosporin auto-resistance, and four
additional genes required for cercosporin biosynthesis, including the final
pathway enzymes that install the unusual cercosporin methylenedioxy bridge. Finally,
we demonstrate production of cercosporin by Colletotrichum
fioriniae, the first known cercosporin producer within this agriculturally
important genus. Thus, our results provide new insight into the intricate
evolution and biology of a toxin critical to agriculture and broaden the
production of cercosporin to another fungal genus containing many plant
pathogens of important crops worldwide.